responses of soil respiration to elevated carbon dioxide

Biogeosciences, 7, 315–328, 2010www.biogeosciences.net/7/315/2010/© Author(s) 2010. This work is distributed underthe Creative Commons Attribution 3.0 License.

Biogeosciences

Responses of soil respiration to elevated carbon dioxide andnitrogen addition in young subtropical forest ecosystems in China

Q. Deng1,2, G. Zhou1, J. Liu1, S. Liu1, H. Duan1,2, and D. Zhang1

1South China Botanical Garden, Chinese Academy of Sciences, Guangzhou 510650, China2Graduate University of Chinese Academy of Sciences, Beijing 100039, China

Received: 16 June 2009 – Published in Biogeosciences Discuss.: 24 August 2009Revised: 28 December 2009 – Accepted: 10 January 2010 – Published: 25 January 2010

Abstract. Global climate change in the real world alwaysexhibits simultaneous changes in multiple factors. Predic-tion of ecosystem responses to multi-factor global changes ina future world strongly relies on our understanding of theirinteractions. However, it is still unclear how nitrogen (N)deposition and elevated atmospheric carbon dioxide concen-tration [CO2] would interactively influence forest floor soilrespiration in subtropical China. We assessed the main andinteractive effects of elevated [CO2] and N addition on soilrespiration by growing tree seedlings in ten large open-topchambers under CO2 (ambient CO2 and 700 µmol mol−1)

and nitrogen (ambient and 100 kg N ha−1 yr−1) treatments.Soil respiration, soil temperature and soil moisture weremeasured for 30 months, as well as above-ground biomass,root biomass and soil organic matter (SOM). Results showedthat soil respiration displayed strong seasonal patterns withhigher values observed in the wet season (April–September)and lower values in the dry season (October–March) in alltreatments. Significant exponential relationships betweensoil respiration rates and soil temperatures, as well as sig-nificant linear relationships between soil respiration ratesand soil moistures (below 15%) were found. Both CO2and N treatments significantly affected soil respiration, andthere was significant interaction between elevated [CO2] andN addition (p < 0.001, p = 0.003, andp = 0.006, respec-tively). We also observed that the stimulatory effect of indi-vidual elevated [CO2] (about 29% increased) was maintainedthroughout the experimental period. The positive effect ofN addition was found only in 2006 (8.17% increased), andthen had been weakened over time. Their combined effecton soil respiration (about 50% increased) was greater than

Correspondence to:D. Zhang([email protected])

the impact of either one alone. Mean value of annual soilrespiration was 5.32± 0.08, 4.54± 0.10, 3.56± 0.03 and3.53± 0.03 kg CO2 m−2 yr−1 in the chambers exposed to el-evated [CO2] and high N deposition (CN), elevated [CO2]and ambient N deposition (CC), ambient [CO2] and high Ndeposition (NN), and ambient [CO2] and ambient N deposi-tion (CK as a control), respectively. Greater above-groundbiomass and root biomass was obtained in the CN, CC andNN treatments, and higher soil organic matter was observedonly in the CN treatment. In conclusion, the combined effectof elevated [CO2] and N addition on soil respiration was ap-parent interaction. They should be evaluated in combinationin subtropical forest ecosystems in China where the atmo-spheric CO2 and N deposition have been increasing simulta-neously and remarkably.

1 Introduction

Soil respiration consists of autotrophic root respiration andheterotrophic respiration which is associated with decompo-sition of litter, roots and soil organic matter (SOM) (Bern-hardt et al., 2006). It is one of the largest fluxes in the globalcarbon cycle (68–75×1015 g C yr−1) (Raich and Schlesinger,1992). Global modeling studies have demonstrated that evena small change in soil CO2 emissions due to global changehas the potential to impact atmosphere CO2 accumulationand global carbon budget (Woodwell et al., 1998 Cox et al.,2000; Cramer et al., 2001). Since global climate change inthe real world always exhibits concurrent changes in multiplefactors (Shaw et al., 2002; Norby and Luo 2004), understand-ing regulations of soil respiration by multiple global changefactors is necessary to project global carbon cycling in thefuture.

Published by Copernicus Publications on behalf of the European Geosciences Union.

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316 Q. Deng et al.: Responses of soil respiration to elevated carbon dioxide in China

The atmospheric carbon dioxide concentration [CO2] hasincreased by approximately 35% during the past decades andis predicted to reach 700 µmol mol−1 by the end of this cen-tury (IPCC, 2001). Numerous experiments have been car-ried out to investigate the responses of soil respiration to el-evated [CO2] (Lin et al., 2001; King et al., 2004; Astrid etal., 2004; Bernhardt et al., 2006; Pregitzer et al., 2008). El-evated [CO2] can reduce diffusive conductance (Pearson etal., 1995; Niklaus et al., 1998) and stomatal conductance ofthe leaves (Saxe et al., 1998), which leads to decreased ratesof canopy transpiration and increased soil moisture in CO2enrichment plots (Bunce, 2004). As a result, soil microbialprocesses such as litter decomposition and nutrient miner-alization were stimulated (Niklaus et al., 1998). Soil respi-ration was closely related to photosynthetic activity (Moy-ano et al., 2008). Elevated [CO2] could enhance photosyn-thetic assimilation rates, and hence increased the above- andbelow-ground biomass production. The increase in below-ground biomass would increase CO2 loss from the soil (Luoet al., 1996; Edwards and Norby, 1999) and enhance carbonrelease into the rhizosphere by root exudation (van Ginkel etal., 2000; Allard et al., 2006). The increase in abovegroundbiomass would produce more litter-fall. All these will con-tribute to higher soil respiration under elevated [CO2] (Zaket al., 2000).

However, in Asia, due to the rapid expansion of industrialand agricultural activities, the use and emission of reactive Nincreased from 14 Tg N yr−1 in 1961 to 68 Tg N yr−1 in 2000and is expected to reach 105 Tg N yr−1 in 2030 (Zheng et al.,2002). Atmospheric N deposition (NH+4 -N and NO−

3 -N) insouthern China has also been increasing remarkably (Gal-loway et al., 2004; Mo et al., 2006, 2007; Chen and Mulder,2007) and reached 30–73 kg N ha−1 yr−1 in precipitation insome subtropical forests (Ma, 1989; Ren et al., 2000; Xu etal., 2001). How the increase of [CO2] would influence soilrespiration under high ambient N deposition in subtropicalforests in China remains unclear.

Plants require more nutrients for plant growth under theelevated CO2 treatments. If increases in photosynthetic car-bon gain under elevated [CO2] are not matched by the in-creases in nutrient supply and/or increases in plant nutrient-use efficiency, the effect of CO2 enrichment to plant growthmay decline or weaken over time (Norby et al., 1986; Mur-ray et al., 2000; Luo et al., 2004; Bernhardt et al., 2006),which also would affect soil respiration. However, soil mois-ture might become lower with increased diffusive conduc-tance and stomatal conductance of the leaves under N addi-tion (Li et al., 2004), which will reduce soil microbial activity(Kucera et al., 1971). N addition also leads to soil acidifica-tion (Huber et al., 2004) especially in tropical forests wherethe soils are often highly acidic, which will further affect soilmicrobial activity and SOM decomposition rate (Andersonand Joergensen, 1997; Kemmitt et al., 2006). In addition,it had been reported that N addition decreased root biomassand soil microbial biomass over time (Mo et al., 2007, 2008).

High N deposition might reduce litter decomposition rate(Mo et al., 2006). As a result, the effects of N addition tosoil respiration are still not conclusive. Both increases, de-creases, and unchanged in soil respiration with N additionsto forest soils have been reported (Bowden et al., 2000 and2004; Burton et al., 2004; Micks et al., 2004; Cleveland andTownsend, 2006; Mo et al., 2007 and 2008). Mo et al. (2007)recently showed that the response of soil respiration to atmo-spheric N deposition may vary depending on the rate of Ndeposition and the degree of initial soil nutrient status. HowN deposition and elevated [CO2] would interactively influ-ence soil respiration in subtropical forests has not been wellinvestigated.

We conducted a two-factor experiment investigating theinteractive effects of elevated [CO2] and N deposition on soilrespiration in young subtropical forest ecosystems. We hy-pothesized that

1. elevated [CO2] would stimulate soil respiration due togreater soil C input;

2. the stimulatory effect would be sustained over time dueto the high ambient N deposition in subtropical China;and

3. the combined effect of elevated [CO2] and N additionwould be greater than the impact of either one alone dueto positive interaction. To test the hypotheses, we mea-sured soil respiration, soil temperature and soil moisturefor 30 months, as well as above-ground biomass, rootbiomass and SOM in an open-top chamber experiment.

2 Materials and methods

2.1 Site description

The experiment was conducted at South China BotanicalGarden, Chinese Academy of Sciences, Guangzhou, China(23◦20′ N and 113◦30′ E). The area is characterized by atypical south subtropical monsoon climate, with annual pre-cipitation ranging from 1600 mm to 1900 mm, of whichnearly 80% falls in the hot-humid wet/rainy season (April–September) and 20% in the dry season (October–March). To-tal annual solar radiation reaches 4.37–4.60 GJ m−2 yr−1 inthe photosynthetic active radiation (PAR) range. The meanannual temperature is 21.5◦C, and the mean relative humid-ity is 77% (Liu et al., 2008).

2.2 Open-top chamber design

Ten open-top chambers were built for this experiment. Each3-m diameter chamber is 3-m tall and 0.7-m deep. Theabove-ground part was wrapped with impermeable and trans-parent plastic sheets, leaving the top of the chamber totally

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Q. Deng et al.: Responses of soil respiration to elevated carbon dioxide in China 317

Table 1. Height and basal diameter of the plant seedlings among all treatments at the beginning of the experiment (mean± standard devia-tions). The treatments are: CK = control, NN = high N, CC = elevated CO2, CN = elevated CO2 + high N.

Parameters Species CN CC NN CK

Height (cm)

Acmena acuminatissima 25.54± 0.47 24.40± 0.57 25.03± 0.84 24.83± 1.09Castanopsis hystrix 67.91± 1.39 68.83± 1.25 64.13± 2.28 68.50± 2.45Ormosia pinnata 19.47± 0.55 18.96± 0.71 18.53± 0.85 18.47± 0.77Pinus massoniana 49.33± 2.33 48.31± 2.18 47.41± 2.16 49.59± 2.42Schima superba 38.04± 1.10 37.23± 1.86 36.34± 1.29 35.94± 1.00Syzygium hancei 58.62± 2.19 58.60± 1.75 59.00± 2.43 60.47± 2.41

Basal diametre (cm)

Acmena acuminatissima 0.28± 0.01 0.26± 0.01 0.27± 0.01 0.28± 0.01Castanopsis hystrix 0.65± 0.03 0.62± 0.02 0.55± 0.02 0.61± 0.02Ormosia pinnata 0.53± 0.01 0.54± 0.01 0.53± 0.02 0.52± 0.02Pinus massoniana 0.59± 0.04 0.58± 0.04 0.59± 0.03 0.57± 0.05Schima superba 0.45± 0.01 0.46± 0.02 0.49± 0.04 0.46± 0.02Syzygium hancei 0.56± 0.02 0.52± 0.02 0.57± 0.02 0.59± 0.03

open. Light intensity in the chamber was 97% of that in openspace and no spectral change was detected. Measured rain-fall intensity was identical inside and outside of the cham-bers and the temperature was not significantly different. Thebelow-ground part was delimited by concrete brick wall thatprevented any lateral or vertical water and/or element fluxeswith the outside surrounding soil. Three holes at the bottomof the wall were connected to a stainless steel water collec-tion box. Holes were capped by a 2-mm net to prevent lossesother than those of leachates. In the treatment chambers withelevated [CO2], the additional CO2 was distributed from aCO2 tank by a transparent pipe with pinholes. A big fan wasconnected to the pipe to ensure equal distribution of CO2 inthe entire chamber. Air was introduced into the chambers viathe fan at an exchange rate of about 1.5 chamber volumesper minute. The CO2 flux from the tank was controlled by aflow meter and the CO2 concentrations in the chambers wereperiodically checked by using a Li-Cor 6400 (Li-COR, Inc.,Lincoln, Nebraska, USA).

The soils used in the experiment were collected from anearby ever-green broad-leaved forest after harvesting from26 February 2005 to 3 March 2005. Simultaneously, the soilwas collected as three different layers (0–20, 20–40 and 40–70 cm depth) that were homogenised separately and used tofill the below-ground part of the chambers. The lateritic soilwith its chemical properties (before the soil was collected)was shown in Liu et al. (2008). On 10 March 2005, oneto two year old seedlings grown in a nursery were trans-planted in the chambers without damaging the roots. All thechambers were planted with 48 randomly selected seedlingswith 8 seedlings each of the following 6 species:Castanop-sis hystrixHook.f. & Thomson ex A.DC,Syzygium han-cei Merr. et Perry,Pinus massonianaLambert,Schima su-perbaGardn. and Champ.,Acmena acuminatissima(Blume)Merr. et Perry, andOrmosia pinnata(Lour.) Merr. These6 species were selected because they are all native and all

widely distributed in southern China. No significant differ-ence in height and basal diameter of the plant seedlings wasfound among all treatments at the beginning of the experi-ment (Table. 1).

2.3 Experiment design

We used a completely randomized design with four treat-ments considering two levels of CO2 and two levels of N.Since we have ten open-top chambers, the replication num-ber for the treatments was not equal. For elevated [CO2] andhigh N deposition (CN), and elevated [CO2] and ambient Ndeposition (CC), 3 chambers were used, respectively. Forambient CO2 and high N deposition (NN), and no treatmentas a control (CK), 2 chambers were used, respectively. Theelevated CO2 treatments were achieved by supplying addi-tional CO2 from a tank until reaching a CO2 concentrationof ca. 700 µmol mol−1 in the chambers. The N addition treat-ments were achieved by spraying seedlings once a week fora total amount of NH4NO3 at 100 kg N ha−1 yr−1. No otherfertilizer was used. Since the walls of the chambers below-ground parts blocked lateral and vertical water fluxes, theseedlings were watered with tap water. All the chambers re-ceived the same amount of water as the CK chambers. Thesetreatments started in April 2005.

2.4 Soil respiration measurement

Four PVC soil collars (80 cm2 in area and 5 cm in height)were permanently installed 3 cm into the soil in each cham-ber in April 2006. The distance between adjacent collarswas more than 50 cm. To eliminate the influence of plantson soil respiration, all living plants in the collars were re-moved one day before soil respiration measurement. From26 June 2006 to 22 December 2008, soil respiration was mea-sured once a week using a Li-Cor 6400 infrared gas analyzer

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(Li-COR, Inc., Lincoln, Nebraska, USA) connected with aLi-Cor 6400-09 soil respiration chamber (9.55 cm diameter)(Li-COR, Inc., Lincoln, Nebraska, USA). The measurementswere made between 9:00 am and 12:00 pm local time. Thesoil respiration chamber (with a foam gasket) was put on thePVC soil collars making an air-tight seal. Soil respirationwas measured three times for each soil collar. Soil respira-tion in a treatment chamber was calculated as the mean offour collar measurements (the measurement at four collars ina chamber differed by less than 5% at any measurement pe-riod). Soil temperature at 5 cm below the soil surface wasalso monitored with a thermocouple sensor attached to therespiration chamber during the soil respiration measurement.Volumetric soil moisture of the top 5 cm soil layer was mea-sured on five random locations within a treatment chamberusing a PMKit (Tang et al., 2006) at the same time when thesoil respiration measurements were being taken.

2.5 Annual soil respiration calculation

Annual or semiannual soil respiration for each treatment wasestimated by summing the products of weekly mean soilrespiration and the number of days between samples. Thesoil respiration measurements made between 9:00 am and12:00 pm represent the daytime averages, based on a studyat a similar site where diurnal pattern of soil respiration wasmeasured (Tang et al., 2006). Because the measurement ofsoil respiration began in 26 June 2006, we only estimatedsemiannual soil respiration from July to December in 2006.

2.6 Above-ground biomass, root biomass and soilorganic matter

Plant height and basal diameter were measured at the timeof planting in early March 2005 and then were assessed fivetimes in August 2005, November 2005, May 2006, Septem-ber 2007 and January 2008. Plant height was measured fromthe soil surface to the tip of the apical bud and the basal di-ameter was assessed at the soil surface. To measure plantbiomass, one tree of each species in every chamber was har-vested in January 2008. This tree was separated into roots,stems and leaves. Tree samples were oven-dried at 60◦Cbefore being weighed. The biomass of each harvested treewas calculated with sample biomass using dry/fresh ratio.Strong correlations among dry biomass for each componentpart, basal area and height existed irrespective of size in treesharvested, which were stated in the equation (Whittake andWoodwell, 1986; Wen et al., 1997):

W = a(D2H)b (1)

WhereW is dry biomass of each tree components includ-ing root, stem and leaf (kg m−2), D is plant basal diameter(cm), H is height (cm), anda,b are regression coefficients.

The biomass of other un-harvested trees was calculated sepa-rately by using their height and basal diameter into the equa-tion above. Here plant biomass is the total biomass of alltrees in a chamber irrespective of species. The above-groundbiomass was the sum of stem and leaf biomass.

Soil samples were collected on November, 2008 to deter-mine soil organic matter (SOM). Three samples (0–20 cmdepth) were collected randomly in each chamber. Eachsample was composted from three cores using a standardsoil probe (2.5 cm inside diameter). The composite sampleswere gently mixed. SOM was determined following WalkleyBlack’s wet digestion method (Nelson and Sommers, 1982).

2.7 Data analysis

Repeated measures ANOVA with Tukey’s HSD test was usedto examine treatment effects (including the main effects ofCO2, N, time-of-season and their interactions) on soil res-piration rate, soil temperature and soil moisture. Repeatedmeasures ANOVA with Tukey’s HSD test was used to exam-ine treatment difference in soil respiration rate, soil temper-ature and soil moisture. Standard t-test was used to test theseasonal difference in means of soil respiration rate, soil tem-perature and soil moisture. To compare the effects among ourthree measured years, One-way ANOVA with Tukey’s HSDtest was used to test the treatment difference in annual orsemiannual soil respiration, as well as root biomass and soilorganic matter.

Both linear and nonlinear regression models were used toexamine the relationship between soil respiration rates andsoil temperature and moisture (Tang et al., 2006; Li et al.,2008). Simple models with soil temperature and soil mois-ture were performed. An exponential equation and a linearequation were used:

R = aexp(bT ) (2)

R = aM +b (3)

WhereR is soil respiration rate (µmol CO2 m−2 s−1), T issoil temperature (◦C), M is soil moisture (%) anda,b areconstants fitted to the regression equation.

The index of soil respiration response to temperature wasalso described by theQ10 value, defined as the difference inrespiration rates over a 10◦C interval.Q10 value was calcu-lated using the exponential relationship between soil respi-ration and soil temperature (Lloyd and Taylor, 1994; Buch-mann, 2000; Xu and Qi, 2001):

Q10= exp(10b) (4)

Whereb is the constant fitted into Eq. 2. One-way ANOVAtest was used to compareb values among treatments.

All analyses were conducted using SPSS 10.0 (SPSS,Chicago, Ill) for Microsoft Windows.



Table 2. Significance of the impacts of CO2 (effect of individual elevated [CO2]), N (effect of individual N addition), CO2*N (the interactiveeffect between elevated [CO2] and N addition) and season on soil respiration (R), soil temperature (T ) and soil moisture (M) in the repeatedmeasures ANOVA.

R T M

F p F p F p

Annual CO2 121.45 < 0.001 0.21 0.643 30.45 < 0.001N 10.31 0.003 0.04 0.846 7.20 0.024CO2*N 7.24 0.006 0.01 0.930 1.95 0.263Season 261.58 < 0.001 520.86 < 0.001 276.11 < 0.001

Wet season CO2 75.25 < 0.001 1.03 0.312 10.01 0.002N 7.26 0.008 0.02 0.898 3.26 0.073CO2*N 0.41 0.524 0.08 0.782 0.39 0.535

Dry season CO2 54.30 < 0.001 0.01 0.906 21.38 < 0.001N 3.47 0.064 0.02 0.881 5.00 0.026CO2*N 18.55 < 0.001 0.01 0.936 1.82 0.179

Table 3. Mean soil respiration rate, mean soil temperature at 5 cm below the soil surface and mean soil moisture of the top 5 cm soil layerunder different CO2 and N treatments (mean± standard deviations). Standard deviation within each treatment showed the dispersion amongopen–top chambers employed for each treatment.n = 3 for the CN and CC treatments,n = 2 for the NN treatment and CK. Mean valueswithin a row with different lowercase letter have significant treatment differences atα=0.05 level. Means values within each column indicatedby the asterisk show significant seasonal differences atα=0.05 level. The treatments are: CK = control, NN = high N, CC = elevated CO2,CN = elevated CO2 + high N.

treatment Time CN CC NN CK

Soil respiration rate Wet season 4.61± 0.10a* 4.12± 0.08b* 3.34± 0.03c* 2.94± 0.05d*(µmol CO2 m−2 s−1) Dry season 2.91± 0.05a* 2.36± 0.03b* 1.89± 0.03c* 2.10± 0.04bc*

Annual means 3.76± 0.07a 3.24± 0.04b 2.56± 0.04c 2.52± 0.02c

Soil temperature (◦C)Wet season 24.20± 0.15a* 25.23± 0.17a* 25.28± 0.11a* 25.25± 0.21a*Dry season 17.26± 0.08a* 17.31± 0.09a* 17.35± 0.13a* 17.33± 0.11a*Annual means 21.23± 0.12a 21.18± 0.11a 21.29± 0.07a 21.25± 0.19a

Soil moisture (%)Wet season 24.31± 0.60a* 25.52± 0.36a* 22.51± 0.76b* 23.48± 0.82ab*Dry season 17.77± 0.64ab* 18.80± 0.24a* 14.72± 0.50c* 17.35± 0.95b*Annual means 20.84± 0.56b 22.16± 0.22a 18.58± 0.90c 20.42± 0.896b

3 Results

3.1 Soil temperature and moisture

Soil temperature and moisture exhibited clear seasonal pat-terns (p < 0.001 for both). Soil was warm and wet fromApril through September (the wet season) and became cooland dry from October to the March of the next year (thedry season) (Tables 2 and 3; Fig. 1). The seasonality ofsoil temperature and moisture was consistent with the sea-sonal patterns of air temperature and precipitation (Liu etal, 2008). Annual mean soil temperature and soil moisturewere 21.25± 0.19◦C and 20.42± 0.90%, respectively in theCK chambers. There was no treatment effect on soil tem-perature (p > 0.05 for all treatments). However, elevated

[CO2] significantly increased soil moisture (p < 0.001), andN addition significantly decreased soil moisture (p = 0.024).The CN treatments did not alter the regimes of soil moisture(P = 0.263) (Tables. 2 and 3).

3.2 Soil respiration

Soil respiration also exhibited a clear seasonal pattern withthe maximum respiration rates occurred during the summerwhen soil temperature and moisture were high; the minimumrespiration rates occurred during the winter when soil tem-perature and moisture were low (p < 0.001 for both) (Ta-ble 3; Fig. 1). In all treatments, significant exponential rela-tionships between soil respiration rate and soil temperature



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Sep-06 Dec-06Mar-07Jun-07 Sep-07 Dec-07Mar-08Jun-08 Sep-08 Dec-08

Fig. 1. Seasonal dynamics of soil temperature at 5 cm below the soil surface, soil moisture of the top 5 cm soil layer and soil respiration rateunder different CO2 and N treatments. The treatments are: CK=control, NN=high N, CC=elevated CO2, CN=elevated CO2 + high N.

were found (p < 0.001 for both) (Table 4; Fig. 2). Temper-ature sensitivity (Q10) was estimated as 1.87, 1.90, 1.86 and1.57 in the CN, CC, NN and CK treatments, respectively.By analyzing subsets of data with low and high soil moisturecontent we found a significant positive linear relationship be-tween soil respiration rate and soil moisture when soil mois-ture was below 15% (Table 4; Fig. 3).

The repeated measures ANOVA showed that bothCO2, N treatments and their interaction affected soilrespiration significantly (F = 121.45, p < 0.001; F =

10.31, p = 0.003; and F = 7.24, p = 0.006, respec-tively) (Table 2). Soil respiration rate was the highestin the CN chambers (3.76± 0.07 µmol CO2 m−2 s−1), fol-lowed by the CC chambers (3.24± 0.04 µmol CO2 m−2 s−1),NN and the control chambers (CK) (2.56± 0.04 and2.52± 0.02 µmol CO2 m−2 s−1, respectively) for the exper-imental period (Table 3). In addition, CO2 treatment af-fected soil respiration significantly in both wet and dry sea-son (p < 0.001, for both), but N treatment affected soil respi-ration significantly only in wet season (p = 0.008) and theirinteraction affected soil respiration significantly only in dryseason (p < 0.001) (Table 2).

The mean value of annual soil respiration was 5.32± 0.08,4.54± 0.10, 3.56± 0.03 and 3.53± 0.03 kg CO2 m−2 yr−1

in the CN, CC, NN and CK treatments, respectively (Ta-ble 5). By analyzing each treatment’s annual or semiannualsoil respiration in the latter half of 2006, 2007 and 2008,we observed that annual or semiannual soil respiration inthe CN and CC treatments increased by 49.24–51.38% and27.24–28.45%, respectively (Table 5). It seems that the stim-ulatory effect of the CN and CC treatments on soil respira-tion was sustained over our study period. However, the ef-fect of the NN treatment on soil respiration was increasedin 2006 (8.17%), with no change in 2007 and 2008 (2.32%and−0.55%, respectively) (Table 5). Obviously, the effectof the NN treatment on soil respiration had been weakenedover time.

3.3 Above-ground biomass, root biomass and soilorganic matter

Both of above- and below-ground biomass in the CN CC andNN treatments was significantly higher than that in the CKchambers at our study sites. Mean above-ground biomasswas 4.37, 3.11, 3.41 and 2.62 kg m−2 in the CN, CC, NN andCK treatment in January 2008, respectively (Fig. 4). Mean



Table 4. Model for relationships between the soil respiration (R) and soil temperature at 5 cm below the soil surface (T ) and soil moisture ofthe top 5 cm soil layer (M) (mean± standard deviations). Standard deviation within each treatment showed the dispersion among open-topchambers employed for each treatment.n = 3 for the CN and CC treatments,n = 2 for the NN treatment and CK. Mean values ofb in theexponential equation (R = aexp(bT)) within a column with different lowercase letter have significant treatment differences atα=0.05 level.R2 is the determination of coefficient. The treatments are: CK = control, NN = high N, CC = elevated CO2, CN = elevated CO2 + high N.Unit: µmol CO2 m−2 s−1 for R; ◦C for T and % forM.

Treatment a b Q10 p R2

a) Soil moisture> 15%:R = aexp(bT )

CN 1.0155± 0.027 0.0627± 0.001 a 1.87 < 0.001 0.68CC 0.8085± 0.061 0.0641± 0.001 a 1.90 < 0.001 0.69NN 0.66± 0.017 0.062± 0.002 a 1.86 < 0.001 0.67CK 0.9904± 0.030 0.0449± 0.001 b 1.57 < 0.001 0.57

Treatment a b n p R2

b) Soil moisture< 15%:R = aM +b

CN 0.1545± 0.007 1.1638± 0.071 13 < 0.001 0.61CC 0.1389± 0.008 0.701± 0.044 10 < 0.001 0.63NN 0.1332± 0.011 0.5926± 0.058 37 < 0.001 0.60CK 0.1651± 0.010 0.3893± 0.055 20 < 0.001 0.54

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y = 0.9144e0.0627x R2 = 0.69 P<0.001 n=96

y = 0.7349e0.0651x R2 = 0.69 P<0.001 n=100

y = 0.6254e0.062x

R2 = 0.67 P<0.001 n=77

y = 0.887e0.0449x

R2 = 0.57 P<0.001 n=90

Fig. 2. Relationships between soil respiration rate and soil temperature at 5 cm depth when soil moisture was larger than 15% under differentCO2 and N treatments. Each datum in panels CN and CC is the mean of three replications. Each datum in panels NN and CK is the mean oftwo replications. The treatments are: CK = control, NN = high N, CC = elevated CO2, CN = elevated CO2 + high N.

root biomass was 1.43, 1.29, 1.17 and 0.91 kg m−2 in theCN, CC, NN and CK treatment in January 2008, respec-tively (Fig. 4). Higher SOM was observed only in the CNtreatment (p < 0.05). There was no significant differenceof SOM among the CC, NN and CK chambers (p > 0.05).Mean SOM was 2.68, 2.17, 2.41 and 2.21%, respectivelyin the CN, CC, NN and CK treatment in November 2008(Fig. 4).

4 Discussion

4.1 Effect of soil temperature and moisture on theseasonality of soil respiration

Soil respiration in all treatments showed strong seasonal pat-terns with higher value observed in the wet season (April–September) compared to the dry season (October–March)(Fig. 1). This is consistent with other results reported in



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5 7 9 11 13 15

0

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Fig. 3. Relationships between soil respiration rate and soil moisture of the top 5 cm soil layer (below 15%) under different CO2 and Ntreatments. Each datum in panels CN and CC is the mean of three replications. Each datum in panels NN and CK is the mean of tworeplications. The treatments are: CK = control, NN = high N, CC = elevated CO2, CN = elevated CO2 + high N.

subtropical forests in China (Tang et al., 2006; Zhang et al.,2006; Mo et al., 2007, 2008). This area is characterized bya typical subtropical monsoon climate, where nearly 80% ofannual precipitation falls in the wet season (April to Septem-ber). Besides, air temperature in the wet season is signif-icantly higher than that in the dry season. Therefore, highplant growth and soil microbial activity in the wet season canstimulate greater soil respiration rate. Positive exponentialrelationships between soil respiration and soil temperature,as well as positive linear relationships between soil respira-tion and soil moisture have been found in some warm andmoist forests (Sotta et al., 2004; Cleveland and Townsend,2006; Tang et al., 2006; Zhang et al., 2006; Mo et al., 2007,2008). In our study, significant exponential relationships be-tween soil respiration rates and soil temperatures were devel-oped when soil moisture was higher than 15% (Fig. 2). Wefound that soil respiration linearly increased with soil mois-ture when soil moisture was below 15% (Fig. 3). A similarresult was reported by Mo et al. (2008) in a mature tropicalforest in southern China. Inclan et al. (2007) believed soilmoisture effects on soil respiration might occur below a cer-tain threshold varying with soil texture (Dilustro et al., 2005).Our result suggested that soil moisture may play a more im-portant role in soil respiration rate as the soil becomes drier.

4.2 Temperature sensitivity of soil respiration

The temperature sensitivity (Q10) of soil respiration was sig-nificantly higher in the CN, CC and NN treatments whencompared to the CK chambers (Table 4 and Fig. 2), suggest-ing that elevated [CO2] and N would increase temperature

sensitivity. This is probably because the CN, CC and NNtreatments increased the allocation of carbon to the roots.Higher SOM was also observed in the CN treatment. Soilrespiration is thought to be controlled primarily by tempera-ture (Lloyd and Taylor, 1994). This is based on the assump-tion that enzymatic rates control soil physiological processesto a greater extent than resource supply rates (Skopp et al.,1990; Craine et al., 1998). Zheng et al. (2009) also reportedthatQ10 of soil respiration was primarily determined by soiltemperature during measurement periods, soil organic car-bon (SOC) content, and ecosystem type. So the respiratorysubstrate availability plays a crucial role in the response ofsoil respiration to soil temperature (Liu et al., 2006). Whensubstrate supply is low, the temperature sensitivity of soil res-piration is low. Otherwise, increased substrate supply canelevate the temperature sensitivity of soil respiration. There-fore, these additional substrates of root biomass and SOM(Fig. 4) for autotrophic and heterotrophic respiration in ourstudy could result in high temperature sensitivity (Dhillion etal., 1996; Lin et al., 2001; Pendall et al., 2004).

4.3 Effect of elevated [CO2] on soil respiration

Many studies indicated that elevated [CO2] increased soilrespiration significantly (Lin et al., 2001; King et al., 2004;Astrid et al., 2004; Bernhardt et al., 2006; Pregitzer et al.,2008). Our results also demonstrated that elevated CO2 re-sulted in a considerable increase of carbon release (about29% on average) from the forest floor. The increase wascomparable to an open-top chamber study in eastern Fin-land which reported about a 30% increase (Sini et al., 2004).



Table 5. Aannual or semiannual soil respiration (R) and its % increased for each year of the experiment (mean± standard deviations).Standard deviation within each treatment showed the dispersion among open-top chambers employed for each treatment.n = 3 for the CNand CC treatments,n = 2 for the NN treatment and CK.R within a row with different lowercase letter have significant treatment differencesat α = 0.05 level. The treatments are: CK = control, NN = high N, CC = elevated CO2, CN = elevated CO2+ high N. % increased = 100((R of each treatment –R of the CK)/R of the CK) % (in the same year). Unit: kg CO2 m−2 6-months−1 for R in the latter half of 2006;kg CO2 m−2 yr−1 for R in 2007 and 2008.

Year∗CN CC NN CK

R % increased R % increased R % increased R

2006 2.72± 0.9a 49.24 2.22± 0.12b 27.24 1.97± 0.10c 8.17 1.83± 0.03d2007 5.16± 0.10a 49.57 4.43± 0.18b 28.41 3.53± 0.10c 2.32 3.45± 0.07c2008 5.48± 0.12a 51.38 4.65± 0.06b 28.45 3.60± 0.05c -0.55 3.62± 0.01cmean 5.32± 0.09a 50.07 4.54± 0.10b 28.61 3.56± 0.03c 0.01 3.53± 0.03c

∗ Because the measurement of soil respiration begun in 26 June 2006, we only estimate semiannual soil respiration from July to Decemberin 2006 and estimate the mean value of all year from 2007 to 2008.

However, it was higher than the Duke Forest Free Air CO2Enrichment (FACE) Experiment (about 16% on average)(Bernhardt et al., 2006) and the FACE Experiment of the Fed-eral Agricultural Research Centre (about 17% on average)(Astrid et al., 2004). The increased soil respiration in the CCchambers may be due to the following two reasons. Firstly,increased soil moisture under elevated [CO2] may increaseSOM decomposition rate and stimulate soil microbial respi-ration. Many studies showed that CO2 enrichment increasedsoil moisture (Amthor, 2001; Bunce 2004). Higher soil mois-ture in the CC treatment was revealed at our study sites (Ta-bles 2 and 3), which would stimulate soil microbial processes(Niklaus et al., 1998) by improving litter decomposition andnutrient mineralization. Secondly, increased root biomassmay increase root respiration and rhizosphere microbial res-piration. Most studies showed that elevated [CO2] increasedfine root biomass and in most cases higher fine turnover re-sulted in higher C input into soil via root necromass (Ed-wards and Norby, 1999; Norby and Luo, 2004; Lukac et al.,2009). In our study, elevated [CO2] increased root biomass(Fig. 4) that was also accompanied by increased CO2 lossfrom the soils.

By analyzing each treatment’s annual or semiannual soilrespiration in the latter half of 2006, 2007 and 2008, we ob-served that the stimulatory effect of elevated [CO2] on soilrespiration was maintained throughout the experimental pe-riod (Table 5). This is not consistent with some other re-ports which showed that soil respiration gradually declinedover time because of the N limitation (e.g., Bernhardt et al.,2006). Increases in photosynthetic carbon gain under el-evated [CO2] need to be matched by increases in nutrientsupply and/or increases in plant nutrient-use efficiency, oth-erwise the effect of CO2 enrichment on plant growth mayweaken due to N-limitation (Norby et al., 1986; Murray etal., 2000). At our study area, the rapid expansion of in-dustrial and agricultural activities in subtropical regions hasresulted in high atmospheric N deposition (NH+

4 -N, NO−

3 -

N) in forests of southern China (30–73 kg N ha−1 yr−1) (Ma,1989; Ren et al., 2000; Xu et al., 2001). It seems that plantgrowth is not limited by N under elevated [CO2] in the longterm. This may be the reason that the stimulatory effect ofelevated [CO2] on soil respiration might be sustained overtime, at least during the current experimental period.

4.4 Effect of N addition on soil respiration

Some other studies showed that soil respiration would besuppressed under N addition (Boxman et al., 1998; Mo etal., 2008). However, the repeated measures ANOVA in ourstudy showed that a positive effect on soil respiration existedin the NN treatment, which may primarily owe to N additionstimulating soil respiration rate at the very start of the exper-iment. This is similar to the pattern observed by Bowden etal. (2004) that N addition could increase soil respiration sig-nificantly in the first 2 years. The response of soil respirationto elevated N deposition was influenced by the degree of ini-tial soil nutrient status (Mo et al., 2007). We also believedthat young seedlings used in this study grew quickly andrequired more soil N, which would lead to a transitory andslight N limitation at our study sites. Increased abovegroundbiomass and increased root biomass (Fig. 4) was obtained inthe N treatment (Duan et al., 2009). As Bowden et al. (2004)suggested, it is likely that added soil carbon from above-and below-ground litter would stimulate heterotrophic res-piration, and greater root biomass enhanced autotrophic res-piration under N addition. Lu et al. (1998) also reported thatthe root respiration rate for seedlings grown at 50 mg L−1 Nconcentration due to increased root biomass was significantlyhigher than for seedlings grown at 10 mg L−1 N.

By analyzing each treatment’s annual or semiannual soilrespiration in the latter half of 2006, 2007 and 2008, we ob-served that the positive effect of N addition treatment existedin the year 2006 and it had been weakened over time. Aber etal. (1989) reported that N additions would initially stimulate



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Fig. 4. Above-ground biomass and root biomass in January 2008,and soil organic matter in November 2008 under different CO2 andN treatments. Error bars are standard deviations, which showed thedispersion among open-top chambers employed for each treatment.n = 3 for the CN and CC treatments,n = 2 for the NN treatment andCK. Different letters denote significant difference between treat-ments. Significant level is set atα = 0.05. The treatments are: CK= control, NN = high N, CC = elevated CO2, CN = elevated CO2 +high N.

soil microbial activity, but would lead to a carbon limitationstate after microbial demand for N was satisfied over time.In addition, plant growth would become slow over time andneeded to assimilate less N from soil. Meanwhile, with largerdoses of N readily available for uptake, energetic costs ofN assimilation may have been reduced. Since a large frac-tion of root respiration is allocated to N assimilation (Bloomet al., 1992), root activity and autotrophic respiration wouldweaken (Bowden et al., 2004). Here we have not direct data

to prove that the root activity and soil microbial activity wereweakening under N addition in our study. However, soil mi-crobial activity was closely related to soil moisture (Kuceraet al., 1971). In our study, N addition significantly decreasedsoil moisture (Table 3), which might be due to the increasedplant growth (Duan et al., 2009) and the increased diffusiveconductance and stomatal conductance of the leaves in theNN chambers (Li et al., 2004; Duan, H. L., unpublisheddata). Since there was a significant positive linear relation-ship between soil respiration rates and soil moisture whensoil moisture was below 15% (Fig. 3), soil respiration wouldgradually be suppressed with drier soil under N addition (Ta-ble 2). Especially in the dry season, for which mean soilmoisture was below 15%, mean soil respiration rate in theNN chambers had a little decrease compared to the CK cham-bers (Table 3). This gradually weakening trend suggestedthat the responses of soil respiration might reverse in the fu-ture under the continued N addition at our study sites.

4.5 Interactive effect of elevated [CO2] and N additionon soil respiration

Increasing atmospheric CO2 and N deposition are two pri-mary and concurrent changes in subtropical China. Elevated[CO2] could maintain increasing plant growth under N ad-dition (Finzi et al., 2002). Elevated [CO2] and N additionaffected each other in stimulating plant growth (Hungate etal., 2003; Luo et al., 2004; de Graaff et al., 2006), whichcould result in potential and complex interactive effects onsoil respiration. Allen and Schlesinger (2004) reported thatN addition could increase soil respiration in FACE soil coresdue to accelerated litter decomposition. However, experi-mental results in the FACE prototype plot (Oren et al., 2001)showed that adding N fertilizer led to reduced soil respirationresponse to elevated [CO2] (Butnor et al., 2003). In addition,Astrid et al. (2004) found that different levels of N fertiliza-tion generally had no effect on soil respiration in ambient andelevated [CO2] rings, because N seemed not to be a control-ling factor in their study sites.

At our studies sites, although there was high ambient Ndeposition, a significant interactive effect between elevated[CO2] and N addition (F = 7.24,p = 0.006) was found, andthe combined effect of them increased soil respiration by50% compared to that in the CK chambers (Table 5). Thismay be because young seedlings used in this study grewquickly and required more soil N. A positive effect on soilrespiration was revealed in the N treatment (Tables 2 and 3),which indicated a transitory and slight N limitation. ThisN limitation would be intensified and prolonged to a certainextent under elevated [CO2], because [CO2] led to greaterphotosynthetic assimilation rates, and required more N fromsoil for plant growth. As a result, the greatest above-groundbiomass, root biomass and SOM were also revealed in theCN treatment at our study sites (Fig. 4). In several OTC



studies with CO2 and N manipulations, poplar seedlings andsaplings (≈1–5 years old) had greater plant growth stimula-tion by elevated [CO2] at high rather than at low N supply af-ter two years in Michigan (Zak et al., 2000) and Italy (Liber-loo et al., 2005) and three years in Iceland (Sigurdson et al.,2001). Higher root biomass could increase root respirationand rhizosphere microbial respiration. Higher SOM wouldprovide additional carbon supplies to decomposers (Zak etal., 2000), which would stimulate heterotrophic respiration.This might be the reason that the response of soil respirationin young subtropical forest ecosystems to elevated [CO2] un-der high N deposition was much stronger than under low Ndeposition.

In addition, varied soil moisture due to CO2 treatmentmay affect soil respiration response to N addition. Soil mi-crobial processes such as litter decomposition and nutrientmineralization were stimulated by soil moisture (Niklaus etal., 1998). At our study, soil respiration was gradually sup-pressed when soil moisture was below 15% (Table 2). Wefound that soil moisture was significantly reduced by N ad-dition alone (Tables 2 and 3), particularly in dry season (allbelow 15%), which also led to reduced soil respiration. Butthis decreased soil moisture was offset by elevated [CO2]. Asa result, soil moisture in the CN treatment was significantlyhigher than that in the NN treatment (Table 3). Thus, the ef-fect of N on soil respiration was enhanced by CO2 treatment,further indicating a strong interactive effect of these two fac-tors on soil respiration.

5 Conclusions

By measuring soil respiration in open-top chambers withyoung subtropical trees under different CO2 and N treat-ments, we estimated main and interactive effects of CO2 andN on soil respiration. Soil respiration displayed strong sea-sonal patterns, with higher values observed in the wet seasonand lower values in the dry season in all treatments, whichwere primarily driven by soil temperature and soil moisture.Both CO2 and N treatments significantly affected soil respi-ration, and there were significant interactions between ele-vated [CO2] and N addition. Soil respiration was the highestin the chambers exposed to elevated [CO2] and high N depo-sition (CN), followed by the chambers exposed to elevated[CO2] and ambient N deposition (CC), ambient [CO2] andhigh N deposition (NN), and ambient [CO2] and ambient Ndeposition (CK as a control). However, the stimulatory ef-fect of elevated [CO2] on soil respiration was sustained overtime because of a high ambient N deposition in subtropicalChina, even under no N addition. In addition, we found thepositive effect of N addition alone had been weakened overtime. These two different trends of CO2 and N on soil respi-ration could lead to a potential and more complex interactiveeffect of elevated [CO2] and N addition on soil respiration

in the future. Studies on source components of soil respira-tion and multiple aspects of soil carbon cycling are needed inlong-term experiment under different CO2 and N treatments.

Acknowledgements.This work was jointly funded by National Sci-ence Fund for Distinguished Young Scholars (30725006), NationalBasic Research Program of China (No.2009CB421101), NationalNatural Science Foundation of China (40730102, 30700112,30721140307), Guangdong Provincial Natural Science Foundationof China (8351065005000001, 7006918) and Dinghushan ForestEcosystem Research Station. We are grateful to Dafeng Hui atTennessee State University, Nashville, TN, USA, for his valuablecomments, and Jennifer Cartwright and Sara Jabeen who provideEnglish improvements.

Edited by: T. Hirano

References

Aber, J. D., Nadelhoffer, K. J., Steudler, P., Melillo, J. M.: Nitrogensaturation in northern forest ecosystems, BioScience, 39, 378–386, 1989.

Allard, V., Robin, C., Newton, P. C. D., Lieffering, M., and Sous-sana, J. F.: Short and long–term effects of elevated CO2 onLolium perennerhizodeposition and its consequences on soil or-ganic matter turnover and plant N yield, Soil Biology and Bio-chemistry, 38(6), 1178–1187, 2006.

Allen, A. S. and Schlesinger, W. H.: Nutrient limitations to soilmicrobial biomass and activity inloblolly pineforests, Soil Biol.Biochem., 36, 581–589, 2004.

Amthor, J. S.: Effects of atmospheric CO2 concentration on wheatyield: review of results from experiments using various ap-proaches to control CO2 concentration, Field Crop. Res., 73, 21–34, 2001.

Anderson, T. H. and Joergensen, G. R.: Relationship between SIRand FE estimates of microbial biomass C in deciduous forest soilat different PH, Soil Biol. Biochem., 29(7), 1033–1042, 1997.

Astrid, R. B., Giesemann, A., Anderson, T. H., Weigel, H. J., andBuchmann, N.: Soil respiration under elevated CO2 and its parti-tioning into recently assimilated and older carbon sources, PlantSoil, 262, 85–94, 2004.

Bernhardt, E. S., Barber, J. J., Pippen, J. S., Taneva, L., Andrews,J. A., and Schlesinger, W. H.: Long-term effects of Free AirCO2 Enrichment (FACE) on soil respiration, Biogeochemistry,77, 91–116, 2006.

Boxman, A. W., Blanck, K., Brandrud, T. E., Emmett, B. A.,Gundersen, P., Hogervorst, R. F., Kjonaas, O. J., Person,H., and Timmermann, V.: Vegetation and soil biota responseto experimentally-changed nitrogen inputs in coniferous forestecosystems of the NITREX project, Forest Ecol. Manag., 101,65–79, 1998.

Bowden, R. D., Davidson, E., Savage, K., Arabia, C., and Steudler,P.: Chronic nitrogen additions reduce total soil respiration andmicrobial respiration in temperate forest soils at the Harvard For-est, Forest Ecol. Manag., 196, 43–56, 2004.

Bowden, R. D., Rullo, G., and Sevens, G. R.: Soil fluxes of carbondioxide, nitrous oxide, and methane at a productive temperatedeciduous forest, J. Environ. Qual., 29, 268–276, 2000.



Buchmann, N.: Biotic and abiotic factors controlling soil respira-tion rates in Picea abies stands, Soil Biology and Biochemistry,32, 1625–1635, 2000.

Bunce, J. A.: Carbon dioxide effects on stomatal responses to theenvironment and water use by crops under field conditions, Oe-cologia, 140, 1–10, 2004.

Burton, A. J., Pregitzer, K., Crawford, J. N., Zogg, G. P., and Zak,D. R.: Simulated chronic NO−3 deposition reduces soil respira-tion in northern hardwood forests, Glob. Change Biol., 10, 1080–1091, 2004.

Butnor, J. R., Johnsen, K. H., Oren, R., and Katul, G. G.: Reductionof forest floor respiration by fertilization on both carbon dioxide-enriched and reference 17-year-old loblolly pine stands, Glob.Change Biol., 9, 849–861, 2003.

Chen, X. Y. and Mulder, J.: Indicators for nitrogen status and leach-ing in subtropical forest ecosystems, South China, Biogeochem-istry, 82, 165–180, 2007.

Cleveland, C. C. and Townsend, A. R.: Nutrient additions to a trop-ical rain forest drive substantial soil carbon dioxide losses to theatmosphere, Proceedings of National Academy of Sciences, 103,10316–10321, 2006.

Contrasting effects of elevated CO2 on old and new soil carbonpools, Soil Biology and Biochemistry, 33, 365–373, 2001.

Cox, P. M., Betts, R. A., Jones, C. D., Spall, S. A., and Totterdell,I. J.: Acceleration of global warming due to carbon–cycle feed-backs in a coupled climate model, Nature, 408, 184–187, 2000.

Craine, J. M., Wedin, D. A., and Chapin, F. S.: Predominance ofecophysiogical controls on soil CO2 flux in a Minnesota grass-land, Plant Soil, 207, 77–86, 1998.

Cramer, W., Bondeau, A., lan Woodward, F., Prentice, C., Betts, A.,Brovkin, V., Cox, P. M., Fisher, V., Foley, J. A., Friend, A. D.,Kucharik, C., Lomas, M. R., Ramankutty, N., Sitch, S., Smith,B., White, A., and Mollong, C. Y.: Global response of terrestrialecosystem structure and function to CO2 and climate change:results from six dynamic global vegetation models, Glob. ChangeBiol., 7(4), 357–373, 2001.

de Graaff, M., van Groenigen, K., Six, J., and van Kessel, C.: In-teractions between plant growth and soil nutrient cycling underelevated CO2: a meta-analysis, Glob. Change Biol., 12, 2077–2091, 2006.

Dhillion, S. C., Roy, J., and Abrams, M.: Assessing the impactof elevated CO2 on soil microbial activity in a Mediterraneanecosystem, Plant Soil, 187, 333–342, 1996.

Duan, H. L., Liu, J. X., Deng, Q., Chen, X. M., and Zhang, D.Q.: Effects of elevated CO2and N deposition on plant biomassaccumulation and allocation in subtropical forest ecosystems: amesocosm study, Chinese Journal of Plant Ecology, (in Chinesewith English abstract), 33(3), 572–579, 2009.

Edwards, N. T. and Norby, R. J.: Below-ground respiratory re-sponses of sugar maple and red maple saplings to atmosphericCO2 enrichment and elevated air temperature, Plant Soil, 206,85–97, 1999.

Finzi, A. C., DeLucia, E. H., Hamilton, J. G., Richter, D. D., andSchlesinger, W. H.: The nitrogen budget of a pine forest underFree Air CO2 Enrichment, Oecologia, 132(4), 567–578, 2002.

Galloway, J. N., Dentener, F. J., and Capone, D. G.: Nitrogen cy-cles: past, present and future, Biogeochemistry, 70, 153–226,2004.

Huber, C., Weis, W., Baumgarten, M., and Gottlein, A.: Spatial andtemporal variation of seepage water chemistry after femel andsmall scale clear-cutting in a N-saturated Norway spure stand,Plant Soil, 267, 23–40, 2004.

Hungate, B. A., Dukes, J. S., Shaw, M. R., and Luo, Y. Q., Field,C. B.: Nitrogen and climate change, Science, 302, 1512–1513,2003.

Inclan, R., de la Torre, D., Benito, M., and Rubio, A.: Soil CO2efflux in a mixed pine-oak forest in Valsain (central Spain), TheScientific World Journal, 7, 166–174, 2007.

Intergovernmental Panel on Climate Change (IPCC).: Land Use,Land Use Change, and Forestry, Cambridge University Press,Cambridge, 1–51, 2001.

Kemmitt, S. J., Wright, D., Goulding, and K. W. T.: PH regulationof carbon and nitrogen dynamics in two agricultural soil, SoilBiology and Biochemistry, 38(5), 898–911, 2006.

King, J. S., Hanson, P. J., Bernhardt, E., Deangeli, P., Norby, R.J., and Pregitzer, K. S.: A multiyear synthesis of soil respirationresponses to elevated atmospheric CO2 from four forest FACEexperiments, Glob. Change Biol., 10, 1027–1042, 2004.

Kucera, C. L. and Kirkham, D. R.: Soil respiration studies in tall-grass prairie in Missouri, Ecology, 52, 912–915, 1971.

Li, D. J., Mo, J. M., Fang, Y. T., Cai, X. A., Xue, J. H., and Xu, G.L.: Effects of simulated nitrogen deposition on growth and pho-tosynthesis ofSchima superba, Castanopsis chinensisandCryp-tocarya concinnaseedlings, Acta Ecologica Sinica, (in Chinesewith English abstract), 24(5), 876–882, 2004.

Li, Y. L., Otieno, D., Owen, Q., Tenhunen, J., Zhang, Y., Lin, Y.B., and Rao X. Q.: Temporal variability in soil CO2 emission inan Orchard forest ecosystem in lower subtropical China, Pedo-sphere, 18, 273–283, 2008.

Liberloo, M., Dillen, S.Y., Calfapietra, C., Marinari, S., Luo, Z.B.,et al.: Elevated CO2 concentration, fertilization and their interac-tion: growth stimulation in a short-rotation poplar coppice (EU-ROFACE), Tree Physiology, 25, 179–89, 2005.

Lin, G., Rygiewicz, P. T., Ehleringer, J. R., Johnson, M. G., andTingey, D. T.: Time-dependent responses of CO2 efflux compo-nents to elevated atmospheric CO2 and temperature in experi-mental forest mesocosms, Plant Soil, 229, 259–270, 2001.

Liu, H. S., Li, L. H., Han, X. G., Huang, J. H., Sun, J. X., andHuang, H. Y.: Respiratory substrate availability plays a crucialrole in the response of soil respiration to environmental factors,Appl. Soil Ecol., 32, 284–292, 2006.

Liu, J. X., Zhang, D. Q., Zhou, G. Y., Benjamin, F. V., Deng, Q.,and Wang, C. L.: CO2 enrichment increases cation and anionloss in leaching water of model forest ecosystems in southernChina, Biogeoscience, 5, 1783–1795, 2008.

Lloyd, J. and Taylor, J. A.: On the temperature dependence of soilrespiration, Funct. Ecol., 8, 315–323, 1994.

Lu, S.J., Mattson, K.G., Zaerr, J.B., et al.: Root respiration ofDouglas-fir seedlings: Effects of N concentration, Soil Biologyand Biochemistry, 30(3), 331–336, 1998.



Luo, Y. Q., Jacson, R. B., Field, C. B., and Mooney, H. A.: ElevatedCO2 increases below ground respiration in California grasslands,Oecologia, 108, 130–137, 1996.

Luo, Y. Q., Su, B., Currie, W. S., Dukes, J. E., Finzi, A., Hartwig,U., Hungate, B., Mc Murtrie, R. E., Oren, R., Parton, W. J.,Pataki, D. E., Rebecca Shaw, M., Zak, D. R., and Field, C. B.:Progressive nitrogen limitation of ecosystem responses to risingatmospheric carbon dioxide, BioScience, 54(8), 731–739, 2004.

Ma, X. H.: Effects of rainfall on the nutrient cycling in manmadeforests of Cunninghamia lanceolata and Pinus massoniana, ActaEcologica Sinica, (in Chinese with English abstract), 9, 15–20,1989.

Lukac, M., Lagomarsino, A., Cristine Moscatelli, M., de Angelis,M., Prancesca Cotrufo, M., and Godbold, D. L.: Forest soil car-bon cycle under elevated CO2–a case of increased throughput?Forestry, 82(1), 75–86, 2009.

Micks, P., Aber, J. D., Boone, R. D., and Davidson, E. A.: Short–term soil respiration and nitrogen immobilization response to ni-trogen applications in control and nitrogen–enriched temperateforests, Forest Ecol. Manag., 196, 57–70, 2004.

Mo, J. M., Brown, S., Xue, J. H., Fang, Y. T., and Li, Z. A.:Response of litter decomposition to simulated N deposition indisturbed, rehabilitated and mature forests in subtropical China,Plant Soil, 282, 135–151, 2006.

Mo, J. M., Zhang, W., Zhu, W. X., Fang, Y. T., Li, D. J., and Zhao,P.: Response of soil respiration to simulated N deposition in adisturbed and a rehabilitated tropical forest in southern China,Plant Soil, 296, 125–135, 2007.

Mo, J. M., Zhang, W., Zhu, W. X., Gundersen, P., Fang, Y. T., Li, D.J., and Wang, H.: Nitrogen addition reduces soil respiration in amature tropical forest in southern China, Glob. Change Biol., 14,403–412, 2008.

Moyano, F. E., Kutsch, W. L., and Rebmann, C.: Soil respirationfluxes in relation to photosynthetic activity in broad-leaf andneedle-leaf forest stands, Agr. Forest Meteorol., 148, 135–143,2008.

Murray, M. B., Smith, R. I., Friend, A., and Jarvis, P. G.: Effect ofelevated [CO2] and varying nutrient application rates on physiol-ogy and biomass accumulation of Sitka spruce (Picea sitchensis),Tree Physiology, 20, 421–434, 2000.

Nelson, D. W. and Sommers, L. E.: Total carbon, organic carbon,and organic matter, 539–580, 1982.

Niklaus, P. A., Spinnler, D., and Kornerb, C.: Soil moisture dynam-ics of calcareous grassland under elevated CO2, Oecologia, 117,201–208, 1998.

Norby, R. J. and Luo, Y. Q.: Evaluating ecosystem responses torising atmospheric CO2 and global warming in a multi-factorworld, New Phytol., 162, 281–293, 2004.

Norby, R. J., O’Neill, E. G., and Luxmoore, R. J.: Effects of atmo-spheric CO2 enrichment on the growth and mineral nutrition ofQuercus albaSeedlings in nutrient-poor soil, Plant Physiol., 82,83–89, 1986.

Oren, R., Ellsworth, D. S., Johnsen, K. H., Phillips, N., Ewers, B.E., Maier, C., Schafer, K. V. R., McCarthy, H., Hendrey, G., Mc-Nulty, S. G., and Katul, G. G.: Soil fertility limits carbon se-questration by forest ecosystems in a CO2-enriched atmosphere,Nature, 411, 469–472, 2001.

Pearson, M., Davies, W. J., and Mansfield, T. A.: Asymmetric re-sponses of adaxial and abaxial stomata to elevated CO2-impacts

on the control of gas-exchange by leaves, Plant Cell and Envi-ronment, 18(8), 837–843, 1995.

Pendall, E., Bridgham, S., Hanson, P. J., Hungate, B., Kicklighter,D. W., Johnson, D. W., Law, B. E., Luo, Y. Q., Megonigal, J.P., Olsrud, M., Ryan, M. G., Wan, S. Q.: Below-ground pro-cess responses to elevated CO2 and temperature: a discussion ofobservations, measurement methods, and models, New Phytol.,162, 311–322, 2004.

Pregitzer, K. S., Burton, A. J., King, J. S., and Zak, D. R.: Soilrespiration, root biomass, and root turnover following long-termexposure of northern forests to elevated atmospheric CO2 andtropospheric O3, New Phytol., 180, 153–161, 2008.

Raich, J. W. and Schlesinger, W. H.: he global carbon dioxide fluxin soil respiration and its relationship to vegetation and climate,Tellus, 44B, 81–99, 1992.

Ren, R., Mi, F. J., and Bai, N. B.: A chemometrics analysis onthe data of precipitation chemistry of China, Journal of BeijingPolytechnic University, (in Chinese with English abstract), 26,90–95, 2000.

Saxe, H., Ellsworth, D. S., and Heath, J.: Tansley Review No. 98Tree and forest functioning in an enriched CO2 atmosphere, NewPhytol., 139, 395–436, 1998.

Shaw, M. R., Zavaleta, E. S., and Chiariello, N. R.: Grassland re-sponses to global environmental changes suppressed be y ele-vated CO2, Science, 298, 1987–1990, 2002.

Sigurdsson, B. D., Thorgeirsson, H., and Linder, S.: Growth anddry-matter partitioning of youngPopulus trichocarpain responseto carbon dioxide concentration and mineral nutrient availability,Tree Physiology, 21, 941–50, 2001.

Sini, M. N., Jouko, S., and Seppo, K.: Soil CO2 efflux in a borealpine forest under atmospheric CO2 enrichment and air warming,Glob. Change Biol., 10, 1363–1376, 2004.

Skopp, J., Jawson, M. D., and Doran, J. W.: Steady-state aerobicmicrobial activity as a function of soil-water content, Soil Sci.Soc. Am. J., 54, 1619–1625, 1990.

Sotta, E. D., Meir, P., Malhi, Y., Nobre, A. D., Hodnett, M., andGrace, J.: Soil CO2 efflux in a tropical forest in the central Ama-zon, Glob. Change Biol., 10, 601–617, 2004.

Tang, X. L., Liu, S. G., Zhou, G. Y., Zhang, D. Q., and Zhou, C.Y.: Soil-atmoshpheric exchange of CO2, CH4 and N2O in threesubtropical forest ecosystems in southern China, Glob. ChangeBiol., 12, 546–560, 2006.

van Ginkel, J. H., Gorissen, A., and Polci, D.: Elevated atmosphericcarbon dioxide concentration: effects of increased carbon inputin a Lolium perennesoil on microorganisms and decomposition,Soil Biology and Biochemistry, 32(4), 449–456, 2000.

Wen, D. Z., Wei, P., Kong, G. H., Zhang, Q. M., and Huang, Z.L.: Biomass study of the community ofCastanopsis chinen-sis+Cryptocarya concinna+Schima superbain a southern Chinareserve, Acta Ecologica Sinica, (in Chinese with English ab-stract), 17(5), 497–504, 1997.

Whittake, R. H. and Woodwell, G. M.: Dimension and productionrelations of trees and shrubs in the Brookhaven forest, New York,J. Ecol., 56, 1–25, 1986.

Xu, Y. G., Zhou, G. Y., Lou, T. S., Wu, Z. M., and He, Z. C.: Soilsolution chemistry and element budget in the forest ecosystemin Guangzhou, Acta Ecologica Sinica, (in Chinese with Englishabstract), 21, 1760–1861, 2001.

Xu, M., and Qi, Y.: Spatial and seasonal variations of Q10 deter-



mined by soil respiration measurements at a Sierra Nevadan for-est, Glob. Biogeochemistry Cy., 15(3), 687–696, 2001.

Zak, D. R., Pregitzer, K. S., King, J. S., and Holmes, W. E.: Ele-vated atmospheric CO2, fine roots and the response of soil microorganisms: a review and hypothesis, New Phytol., 147, 201–222,2000.

Zhang, D. Q., Sun, X. M., Zhou, G. Y., Yan, J. H., Wang, Y. S., Liu,S. Z., Zhou, C. Y., Liu, J. S., Tang, X. L., Li, J., and Zhang, Q.M.: Seaaonal dynamics of soil CO2 effluxes with responses toenvironmental factors in lower subtropical forest of China, Sci-ence in China Series, Dokl. Earth Sci., 49 (Suppl. II), 139–149,2006.

Zheng, X. H., Fu, C. B., Xu, X. K., Yan, X. D., Huang, Y., Han, S.H., Hu, F., and Chen, G. X.: The Asian nitrogen cycle case study,AMBIO, 31, 79–87, 2002.

Zheng, Z. M., Yu, G. R., Fu, Y. L., Wang, Y. S., Sun, X. M., andWang, Y. H.: Temperature sensitivity of soil respiration is af-fected by prevailing climatic conditions and soil organic carboncontent: A trans–China based case study, Soil Biology and Bio-chemistry, 41, 1531–1540, 2009.


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